Spermine and spermidine inhibit or induce programmed cell death in Arabidopsis thaliana in vitro and in vivo in a dose-dependent manner

FEBS J. 2024 Aug;291(16):3665-3685. doi: 10.1111/febs.17165. Epub 2024 May 29.

Abstract

Polyamines are ubiquitous biomolecules with a number of established functions in eukaryotic cells. In plant cells, polyamines have previously been linked to abiotic and biotic stress tolerance, as well as to the modulation of programmed cell death (PCD), with contrasting reports on their pro-PCD and pro-survival effects. Here, we used two well-established platforms for the study of plant PCD, Arabidopsis thaliana suspension cultures cells and the root hair assay, to examine the roles of the polyamines spermine and spermidine in the regulation of PCD. Using these systems for precise quantification of cell death rates, we demonstrate that both polyamines can trigger PCD when applied exogenously at higher doses, whereas at lower concentrations they inhibit PCD induced by both biotic and abiotic stimuli. Furthermore, we show that concentrations of polyamines resulting in inhibition of PCD generated a transient ROS burst in our experimental system, and activated the expression of oxidative stress- and pathogen response-associated genes. Finally, we examined PCD responses in existing Arabidopsis polyamine synthesis mutants, and identified a subtle PCD phenotype in Arabidopsis seedlings deficient in thermo-spermine. The presented data show that polyamines can have a role in PCD regulation; however, that role is dose-dependent and consequently they may act as either inhibitors, or inducers, of PCD in Arabidopsis.

Keywords: Arabidopsis cell suspension culture; plant programmed cell death; polyamines; root hair assay; spermidine; spermine.

MeSH terms

  • Apoptosis* / drug effects
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Arabidopsis* / drug effects
  • Arabidopsis* / genetics
  • Arabidopsis* / metabolism
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • Gene Expression Regulation, Plant / drug effects
  • Oxidative Stress / drug effects
  • Plant Roots / drug effects
  • Plant Roots / genetics
  • Plant Roots / growth & development
  • Plant Roots / metabolism
  • Reactive Oxygen Species* / metabolism
  • Spermidine* / metabolism
  • Spermidine* / pharmacology
  • Spermine* / metabolism
  • Spermine* / pharmacology

Substances

  • Spermidine
  • Spermine
  • Reactive Oxygen Species
  • Arabidopsis Proteins